Environmental Geochemistry and Health

, Volume 41, Issue 5, pp 2365–2379 | Cite as

Zinc biofortification of cereals—role of phosphorus and other impediments in alkaline calcareous soils

  • Muhammad Akhtar
  • Sundas YousafEmail author
  • Nadeem Sarwar
  • Saddam HussainEmail author
Review Paper


Alkaline calcareous soils are deficient in plant nutrients; in particular, phosphorus (P) and zinc (Zn) are least available; their inorganic fertilizers are generally applied to meet the demand of crops. The applied nutrients react with soil constituents as well as with each other, resulting in lower plant uptake. Phosphorus availability is usually deterred due to lime content, while Zn availability is largely linked with alkalinity of the soil. The present manuscript critically discusses the factors associated with physicochemical properties of soil and other interactions in soil–plant system which contribute to the nutrients supply from soil, and affect productivity and quality attributes of cereals. Appropriate measures may possibly lessen the severity of nutritional disorder in cereal and optimize P and Zn concentrations in grain. Foliar Zn spray is found to escape most of the soil reactions; thus, Zn bioavailability is higher either through increase in grain Zn or through decrease in phytate content. The reactivity of nutrients prior to its uptake is deemed as major impediments in Zn biofortification of cereals. The article addresses physiological limitation of plants to accumulate grain Zn and the ways to achieve biofortification in cereals, while molecular mechanism explains how it affects nutritional quality of cereals. Moreover, it highlights the desirable measures for enhancing Zn bioavailability, e.g., manipulation of genetic makeup for efficient nutrient uptake/translocation, and also elucidates agronomic measures that help facilitate Zn supply in soil for plant accumulation.


Zinc fortification Soil pH Calcareous soil Plant genetic makeup Phytate-to-Zn ratio 



  1. Alloway, B. (1995). Heavy metals in soils. London: Blackie Academic and Professional.Google Scholar
  2. Alloway, B. (2008). Zinc in soils and crop nutrition. In 2nd International Zinc Association (IZN) and International Fertilizer Industry Association (IFIA) Brussels, Belgium.Google Scholar
  3. Alloway, B. (2009). Soil factors associated with zinc deficiency in crops and humans. Environmental Geochemistry and Health, 31, 537–548.Google Scholar
  4. Assunção, A. G., et al. (2010). Arabidopsis thaliana transcription factors bZIP19 and bZIP23 regulate the adaptation to zinc deficiency. Proceedings of the National Academy of Sciences, 107, 10296–10301.Google Scholar
  5. Aulakh, M. S., & Malhi, S. S. (2005). Interactions of nitrogen with other nutrients and water: Effect on crop yield and quality, nutrient use efficiency, carbon sequestration, and environmental pollution. Advances in Agronomy, 86, 341–409.Google Scholar
  6. Bagci, S., Ekiz, H., Yilmaz, A., & Cakmak, I. (2007). Effects of zinc deficiency and drought on grain yield of field-grown wheat cultivars in Central Anatolia. Journal of Agronomy and Crop Science, 193, 198–206.Google Scholar
  7. Barak, P., & Helmke, P. A. (1993). The chemistry of zinc. In A. D. Robson (Ed.), Zinc in soils and plants (pp. 1–13). Dordrecht: Springer.Google Scholar
  8. Barrow, N. (1987). The effects of phosphate on zinc sorption by a soil. European Journal of Soil Science, 38, 453–459.Google Scholar
  9. Bashir, K., Inoue, H., Nagasaka, S., Takahashi, M., Nakanishi, H., Mori, S., et al. (2006). Cloning and characterization of deoxymugineic acid synthase genes from graminaceous plants. Journal of Biological Chemistry, 281, 32395–32402.Google Scholar
  10. Bashir, K., & Nishizawa, N. K. (2006). Deoxymugineic acid synthase: A gene important for Fe-acquisition and homeostasis. Plant Signaling & Behavior, 1, 290–292.Google Scholar
  11. Bhowmik, D., & Chiranjib, K. (2010). A potential medicinal importance of zinc in human health and chronic. International Journal of Pharmaceutics, 1, 05–11.Google Scholar
  12. Bouis, H. E., & Welch, R. M. (2010). Biofortification—A sustainable agricultural strategy for reducing micronutrient malnutrition in the global south. Crop Science, 50, S-20–S-32.Google Scholar
  13. Broadley, M. R., White, P. J., Hammond, J. P., Zelko, I., & Lux, A. (2007). Zinc in plants. New Phytologist, 173, 677–702.Google Scholar
  14. Broadley, M., et al. (2010). Shoot zinc (Zn) concentration varies widely within Brassica oleracea L. and is affected by soil Zn and phosphorus (P) levels. The Journal of Horticultural Science & Biotechnology, 85, 375–380.Google Scholar
  15. Buerkert, A., Haake, C., Ruckwied, M., & Marschner, H. (1998). Phosphorus application affects the nutritional quality of millet grain in the Sahel. Field Crops Research, 57, 223–235.Google Scholar
  16. Buescher, E., et al. (2010). Natural genetic variation in selected populations of Arabidopsis thaliana is associated with ionomic differences. PLoS ONE, 5, e11081.Google Scholar
  17. Cakmak, I. (2000). Possible roles of zinc in protecting plant cells from damage by reactive oxygen species. New Phytologist, 146, 185–205.Google Scholar
  18. Cakmak, I. (2004). Identification and correction of widespread zinc deficiency in turkey: A success storyA NATO-science for Stability Project. International Fertiliser Society.Google Scholar
  19. Cakmak, I. (2008). Zinc deficiency in wheat in Turkey. In B. J. Alloway (Ed.), Micronutrient deficiencies in global crop production (pp. 181–200). Dordrecht: Springer.Google Scholar
  20. Cakmak, I. (2009). Enrichment of fertilizers with zinc: An excellent investment for humanity and crop production in India. Journal of Trace Elements in Medicine and Biology, 23, 281–289.Google Scholar
  21. Cakmak, S., Gülüt, K. Y., Marschner, H., & Graham, R. D. (1994a). Effect of zinc and iron deficiency on phytosiderophore release in wheat genotypes differing in zinc efficiency. Journal of Plant Nutrition, 17, 1–17.Google Scholar
  22. Cakmak, I., Hengeler, C., & Marschner, H. (1994b). Changes in phloem export of sucrose in leaves in response to phosphorus, potassium and magnesium deficiency in bean plants. Journal of Experimental Botany, 45, 1251–1257.Google Scholar
  23. Cakmak, I., & Marschner, H. (1986). Mechanism of phosphorus-induced zinc deficiency in cotton. I. Zinc deficiency-enhanced uptake rate of phosphorus. Physiologia Plantarum, 68, 483–490.Google Scholar
  24. Cakmak, I., & Marschner, H. (1987). Mechanism of phosphorus-induced zinc deficiency in cotton. III. Changes in physiological availability of zinc in plants is mail. Physiologia Plantarum, 70, 13–20.Google Scholar
  25. Cakmak, I., et al. (1997). Differential response of rye, triticale, bread and durum wheats to zinc deficiency in calcareous soils. Plant and Soil, 188, 1–10.Google Scholar
  26. Cakmak, I., et al. (2010). Biofortification and localization of zinc in wheat grain. Journal of Agricultural and Food Chemistry, 58, 9092–9102.Google Scholar
  27. Çakmak, İ., et al. (2004). Triticum dicoccoides: An important genetic resource for increasing zinc and iron concentration in modern cultivated wheat. Soil Science and Plant Nutrition, 50, 1047–1054.Google Scholar
  28. Calderini, D. F., & Ortiz-Monasterio, I. (2003). Grain position affects grain macronutrient and micronutrient concentrations in wheat. Crop Science, 43, 141–151.Google Scholar
  29. Chaney, R. L., Agle, J. S., McIntosh, M. S., Reeves, R. D., Li, Y. M., Brewer, E. P., et al. (2005). Using hyperaccumulator plants to phytoextract soil Ni and Cd. Zeitschrift für Naturforschung C, 60, 190–198.Google Scholar
  30. Chasapis, C. T., Loutsidou, A. C., Spiliopoulou, C. A., & Stefanidou, M. E. (2012). Zinc and human health: An update. Archives of Toxicology, 86, 521–534.Google Scholar
  31. Chaudhry, F., & Loneragan, J. (1970). Effects of nitrogen, copper, and zinc fertilizers on the copper and zinc nutrition of wheat plants. Crop and Pasture Science, 21, 865–879.Google Scholar
  32. Choppala, G., et al. (2014). Cellular mechanisms in higher plants governing tolerance to cadmium toxicity. Critical Reviews in Plant Sciences, 33, 374–391.Google Scholar
  33. Clemens, S., Kim, E. J., Neumann, D., & Schroeder, J. I. (1999). Tolerance to toxic metals by a gene family of phytochelatin synthases from plants and yeast. The EMBO journal, 18, 3325–3333.Google Scholar
  34. Distelfeld, A., et al. (2007). Multiple QTL-effects of wheat Gpc-B1 locus on grain protein and micronutrient concentrations. Physiologia Plantarum, 129, 635–643.Google Scholar
  35. Drakakaki, G., et al. (2005). Endosperm-specific co-expression of recombinant soybean ferritin and Aspergillus phytase in maize results in significant increases in the levels of bioavailable iron. Plant Molecular Biology, 59, 869–880.Google Scholar
  36. Drissi, S., Houssa, A. A., Bamouh, A., Coquant, J.-M., & Benbella, M. (2015). Effect of zinc-phosphorus interaction on corn silage grown on sandy soil. Agriculture, 5, 1047–1059.Google Scholar
  37. Ekiz, H., Bagci, S., Kiral, A., Eker, S., Gültekin, I., Alkan, A., & Cakmak, I. (1998). Effects of zinc fertilization and irrigation on grain yield and zinc concentration of various cereals grown in zinc-deficient calcareous soils. Journal of Plant Nutrition, 21, 2245–2256.Google Scholar
  38. Erdal, I., Yilmaz, A., Taban, S., Eker, S., Torun, B., & Cakmak, I. (2002). Phytic acid and phosphorus concentrations in seeds of wheat cultivars grown with and without zinc fertilization. Journal of Plant Nutrition, 25, 113–127.Google Scholar
  39. Evans, D., & Miller, M. (1988). Vesicular–arbuscular mycorrhizas and the soil-disturbance-induced reduction of nutrient absorption in maize. New Phytologist, 110, 67–74.Google Scholar
  40. Fageria, N., Filho, M. B., Moreira, A., & Guimarães, C. (2009). Foliar fertilization of crop plants. Journal of plant nutrition, 32, 1044–1064.Google Scholar
  41. Freeman, J. L., Zhang, L. H., Marcus, M. A., Fakra, S., McGrath, S. P., & Pilon-Smits, E. A. (2006). Spatial imaging, speciation, and quantification of selenium in the hyperaccumulator plants Astragalus bisulcatus and Stanleya pinnata. Plant Physiology, 142, 124–134.Google Scholar
  42. Graham, R. D., Ascher, J. S., & Hynes, S. C. (1992). Selecting zinc-efficient cereal genotypes for soils of low zinc status. Plant and Soil, 146, 241–250.Google Scholar
  43. Graham, R., Senadhira, D., Beebe, S., Iglesias, C., & Monasterio, I. (1999). Breeding for micronutrient density in edible portions of staple food crops: Conventional approaches. Field Crops Research, 60, 57–80.Google Scholar
  44. Grotz, N., Fox, T., Connolly, E., Park, W., Guerinot, M. L., & Eide, D. (1998). Identification of a family of zinc transporter genes from Arabidopsis that respond to zinc deficiency. Proceedings of the National Academy of Sciences, 95, 7220–7224.Google Scholar
  45. Grotz, N., & Guerinot, M. L. (2006). Molecular aspects of Cu, Fe and Zn homeostasis in plants. Biochimica et Biophysica Acta (BBA)-Molecular Cell Research, 1763, 595–608.Google Scholar
  46. Guerinot, M. L. (2000). The ZIP family of metal transporters. Biochimica et Biophysica Acta (BBA)-Biomembranes, 1465, 190–198.Google Scholar
  47. Guttieri, M., Peterson, K., & Souza, E. (2006). Agronomic performance of low phytic acid wheat. Crop Science, 46, 2623–2629.Google Scholar
  48. Hall, J., & Williams, L. E. (2003). Transition metal transporters in plants. Journal of Experimental Botany, 54, 2601–2613.Google Scholar
  49. Harris, D., Rashid, A., Miraj, G., Arif, M., & Yunas, M. (2008). ‘On-farm’ seed priming with zinc in chickpea and wheat in Pakistan. Plant and Soil, 306, 3–10.Google Scholar
  50. Hotz, C., & Brown, K. H. (2004). Assessment of the risk of zinc deficiency in populations and options for its control. International Nutrition Foundation: For UNU.Google Scholar
  51. Hotz, C., & Gibson, R. S. (2007). Traditional food-processing and preparation practices to enhance the bioavailability of micronutrients in plant-based diets. The Journal of nutrition, 137, 1097–1100.Google Scholar
  52. Huang, C., Barker, S. J., Langridge, P., Smith, F. W., & Graham, R. D. (2000). Zinc deficiency up-regulates expression of high-affinity phosphate transporter genes in both phosphate-sufficient and-deficient barley roots. Plant Physiology, 124, 415–422.Google Scholar
  53. Imran, M., Rehim, A., Sarwar, N., & Hussain, S. (2016). Zinc bioavailability in maize grains in response of phosphorous–zinc interaction. Journal of Plant Nutrition and Soil Science, 179, 60–66.Google Scholar
  54. Ishimaru, Y., Bashir, K., & Nishizawa, N. K. (2011). Zn uptake and translocation in rice plants. Rice, 4, 21–27.Google Scholar
  55. Ishimaru, Y., Suzuki, M., Tsukamoto, T., Suzuki, K., Nakazono, M., Kobayashi, T. (2006). Rice plants take up iron as an Fe3+-phytosiderophore and as Fe2+. The Plant Journal, 45, 335–346.Google Scholar
  56. Ishimaru, Y., et al. (2010). Rice metal-nicotianamine transporter, OsYSL2, is required for the long-distance transport of iron and manganese. The Plant Journal, 62, 379–390.Google Scholar
  57. Kochian, L. V. (1991). Mechanisms of micronutrient uptake and translocation in plants. Micronutrients in Agriculture, 28, 229–296.Google Scholar
  58. Krebs, N. F. (2013). Update on zinc deficiency and excess in clinical pediatric practice. Annals of Nutrition & Metabolism, 62, 19–29.Google Scholar
  59. Lambert, D., Baker, D. E., & Cole, H. (1979). The role of mycorrhizae in the interactions of phosphorus with zinc, copper, and other elements. Soil Science Society of America Journal, 43, 976–980.Google Scholar
  60. Lantican, M. A., Prabhu, L. P., & Rajaram, S. (2003). Is research on marginal lands catching up? The case of unfavourable wheat growing environments. Agricultural Economics, 29, 353–361.Google Scholar
  61. Lasat, M. M., Pence, N. S., Garvin, D. F., Ebbs, S. D., & Kochian, L. V. (2000). Molecular physiology of zinc transport in the Zn hyperaccumulator Thlaspi caerulescens. Journal of Experimental Botany, 51, 71–79.Google Scholar
  62. Lee, J.-Y., Nagano, Y., Taylor, J. P., Lim, K. L., & Yao, T.-P. (2010). Disease-causing mutations in parkin impair mitochondrial ubiquitination, aggregation, and HDAC6-dependent mitophagy. The Journal of Cell Biology: JCB, 189, 671–679.Google Scholar
  63. Lehmann, A., Veresoglou, S. D., Leifheit, E. F., & Rillig, M. C. (2014). Arbuscular mycorrhizal influence on zinc nutrition in crop plants—A meta-analysis. Soil Biology & Biochemistry, 69, 123–131.Google Scholar
  64. Lindsay, W. (1972). Zinc in soils and plant nutrition. Advances in Agronomy, 24, 147–186.Google Scholar
  65. Loneragan, J., Grove, T., Robson, A., & Snowball, K. (1979). Phosphorus toxicity as a factor in zinc–phosphorus interactions in plants. Soil Science Society of America Journal, 43, 966–972.Google Scholar
  66. Loneragan, J., Grunes, D., Welch, R., Aduayi, E., Tengah, A., Lazar, V., et al. (1982). Phosphorus accumulation and toxicity in leaves in relation to zinc supply. Soil Science Society of America Journal, 46, 345–352.Google Scholar
  67. Lott, J. N., & Spitzer, E. (1980). X-ray analysis studies of elements stored in protein body globoid crystals of Triticum grains. Plant Physiology, 66, 494–499.Google Scholar
  68. Maret, W., & Li, Y. (2009). Coordination dynamics of zinc in proteins. Chemical Reviews, 109, 4682–4707.Google Scholar
  69. Marschner, H. (1993). Zinc uptake from soils. In A. D. Robson (Ed.), Zinc in soils and plants (pp. 59–77). Dordrecht: Springer.Google Scholar
  70. Marschner, H. (1995). Mineral nutrition of higher plants (2nd ed., p. 889). Academic Press, London.Google Scholar
  71. Marschner, H., & Schropp, A. (1977). Vergleichende Untersuchungen uber die Empfindlichkeit von 6 Unterlagensorten der Weinrebe gegenuber Phosphat induziertem Zink Mangel Vitis.Google Scholar
  72. Mäser, P., et al. (2001). Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiology, 126, 1646–1667.Google Scholar
  73. Masuda, H., Usuda, K., Kobayashi, T., Ishimaru, Y., Kakei, Y., Takahashi, M. (2009). Overexpression of the barley nicotianamine synthase gene HvNAS1 increases iron and zinc concentrations in rice grains. Rice, 2, 155–166.Google Scholar
  74. Masuda, H., et al. (2008). Increase in iron and zinc concentrations in rice grains via the introduction of barley genes involved in phytosiderophore synthesis. Rice, 1, 100–108.Google Scholar
  75. Moreau, R. A., Whitaker, B. D., & Hicks, K. B. (2002). Phytosterols, phytostanols, and their conjugates in foods: Structural diversity, quantitative analysis, and health-promoting uses. Progress in Lipid Research, 41, 457–500.Google Scholar
  76. Morris, E. R., & Ellis, R. (1989). Usefulness of the dietary phytic acid/zinc molar ratio as an index of zinc bioavailability to rats and humans. Biological Trace Element Research, 19, 107–117.Google Scholar
  77. Mortvedt, J. J., & Authority, T. V. (1991). Compatibility of micronutrients in starter fertilizers. In Starter fertilizer for crops in the southeast: Proceedings of a conference (p. 20). The Institute.Google Scholar
  78. Moussavi-Nik, M., Rengel, Z., Pearson, J., & Hollamby, G. (1997). Dynamics of nutrient remobilisation from seed of wheat genotypes during imbibition, germination and early seedling growth. Plant and Soil, 197, 271–280.Google Scholar
  79. Oltmans, S. E., Fehr, W. R., Welke, G. A., Raboy, V., & Peterson, K. L. (2005). Agronomic and seed traits of soybean lines with low-phytate phosphorus. Crop Science, 45, 593–598.Google Scholar
  80. Ova, E. A., Kutman, U. B., Ozturk, L., & Cakmak, I. (2015). High phosphorus supply reduced zinc concentration of wheat in native soil but not in autoclaved soil or nutrient solution. Plant and Soil, 393, 147–162.Google Scholar
  81. Ozturk, L., et al. (2006). Concentration and localization of zinc during seed development and germination in wheat. Physiologia Plantarum, 128, 144–152.Google Scholar
  82. Peleg, Z., Saranga, Y., Yazici, A., Fahima, T., Ozturk, L., & Cakmak, I. (2008). Grain zinc, iron and protein concentrations and zinc-efficiency in wild emmer wheat under contrasting irrigation regimes. Plant and Soil, 306, 57–67.Google Scholar
  83. Prentice, A. M., Gershwin, M. E., Schaible, U. E., Keusch, G. T., Victora, C. G., & Gordon, J. I. (2008). New challenges in studying nutrition-disease interactions in the developing world. The Journal of Clinical Investigation, 118, 1322–1329.Google Scholar
  84. Qu, L. Q., Yoshihara, T., Ooyama, A., Goto, F., & Takaiwa, F. (2005). Iron accumulation does not parallel the high expression level of ferritin in transgenic rice seeds. Planta, 222, 225–233.Google Scholar
  85. Rahimi, A., & Schropp, A. (1984). Carboanhydrase-Aktivität und extrahierbares Zink als Maßstab für die Zink-Versorgung von Pflanzen. Journal of Plant Nutrition and Soil Science, 147, 572–583.Google Scholar
  86. Ramesh, S. A., Choimes, S., & Schachtman, D. P. (2004). Over-expression of an Arabidopsis zinc transporter in Hordeum vulgare increases short-term zinc uptake after zinc deprivation and seed zinc content. Plant Molecular Biology, 54, 373–385.Google Scholar
  87. Rascio, N., & Navari-Izzo, F. (2011). Heavy metal hyperaccumulating plants: How and why do they do it? And what makes them so interesting? Plant Science, 180, 169–181.Google Scholar
  88. Rashid, A. (2006). Incidence, diagnosis and management of micronutrient deficiencies in crops: Success stories and limitations in Pakistan. In: Proc. IFA Int Workshop on Micronutrients, 2006.Google Scholar
  89. Rattan, R., & Deb, D. (1981). Self-diffusion of zinc and iron in soils as affected by pH, CaCO3, moisture, carrier and phosphorus levels. Plant and Soil, 63, 377–393.Google Scholar
  90. Refuerzo, L., Mercado, E., Arceta, M., Sajese, A., Gregorio, G., & Singh, R. (2009). QTL mapping for zinc deficiency tolerance in rice (Oryza sativa L.). Philippine Journal of Crop Science, 34, 86.Google Scholar
  91. Rehman, H., Aziz, T., Farooq, M., Wakeel, A., & Rengel, Z. (2012). Zinc nutrition in rice production systems: A review. Plant and Soil, 361, 203–226.Google Scholar
  92. Robson, A., & Pitman, M. (1983). Interactions between nutrients in higher plants. In A. Läuchli & R. L. Bieleski (Eds.), Inorganic plant nutrition (pp. 147–180). Berlin: Springer.Google Scholar
  93. Rugh, C. L., Senecoff, J. F., Meagher, R. B., & Merkle, S. A. (1998). Development of transgenic yellow poplar for mercury phytoremediation. Nature Biotechnology, 16, 925–928.Google Scholar
  94. Saifullah, Sarwar N., Bibi, S., Ahmad, M., & Ok, Y. S. (2014). Effectiveness of zinc application to minimize cadmium toxicity and accumulation in wheat (Triticum aestivum L.). Environmental Earth Sciences, 71, 1663–1672.Google Scholar
  95. Santa María, G. E., & Cogliatti, D. H. (1988). Bidirectional Zn-fluxes and compartmentation in wheat seedling roots. Journal of Plant Physiology, 132, 312–315.Google Scholar
  96. Sarkar, A., & Wyn Jones, R. (1982). Influence of rhizosphere on the nutrient status of dwarf French beans. Plant and Soil, 64, 369–380.Google Scholar
  97. Sarwar, N., Ishaq, W., Farid, G., Shaheen, M. R., Imran, M., Geng, M., et al. (2015). Zinc–cadmium interactions: Impact on wheat physiology and mineral acquisition. Ecotoxicology and Environmental Safety, 122, 528–536.Google Scholar
  98. Sarwar, N., Malhi, S. S., Zia, M. H., Naeem, A., Bibi, S., & Farid, G. (2010). Role of mineral nutrition in minimizing cadmium accumulation by plants. Journal of the Science of Food and Agriculture, 90, 925–937.Google Scholar
  99. Sarwar, N., et al. (2017). Phytoremediation strategies for soils contaminated with heavy metals: Modifications and future perspectives. Chemosphere, 171, 710–721.Google Scholar
  100. Schachtman, D. P., & Barker, S. J. (1999). Molecular approaches for increasing the micronutrient density in edible portions of food crops. Field Crops Research, 60, 81–92.Google Scholar
  101. Sillanpää, M. (1982). Micronutrients and the nutrient status of soils: a global study. Food Agriculture Organization, 48, 444.Google Scholar
  102. Singh, B., Natesan, S. K, A., Singh, B., & Usha, K. (2005). Improving zinc efficiency of cereals under zinc deficiency. Current Science, 88, 36–44.Google Scholar
  103. Singh, J., Karamanos, R., & Stewart, J. (1988). The mechanism of phosphorus-induced zinc deficiency in bean (Phaseolus vulgaris L.). Canadian Journal of Soil Science, 68, 345–358.Google Scholar
  104. Somasundar, P., Riggs, D. R., Jackson, B. J., Cunningham, C., Vona-Davis, L., & McFadden, D. W. (2005). Inositol hexaphosphate (IP6): A novel treatment for pancreatic cancer 1. Journal of Surgical Research, 126, 199–203.Google Scholar
  105. Stein, A. J. (2010). Global impacts of human mineral malnutrition. Plant and Soil, 335, 133–154.Google Scholar
  106. Subramanian, K., Balakrishnan, N., & Senthil, N. (2013). Mycorrhizal symbiosis to increase the grain micronutrient content in maize. Australian Journal of Crop Science, 7, 900.Google Scholar
  107. Subramanian, K. S., Bharathi, C., & Jegan, A. (2008). Response of maize to mycorrhizal colonization at varying levels of zinc and phosphorus. Biology and fertility of soils, 45, 133–144.Google Scholar
  108. Suzuki, M., et al. (2006). Biosynthesis and secretion of mugineic acid family phytosiderophores in zinc-deficient barley. The Plant Journal, 48, 85–97.Google Scholar
  109. Sylvia, D., Hammond, L., Bennett, J., Haas, J., & Linda, S. (1993). Field response of maize to a VAM fungus and water management. Agronomy Journal, 85, 193–198.Google Scholar
  110. Tapiero, H., & Tew, K. D. (2003). Trace elements in human physiology and pathology: Zinc and metallothioneins. Biomedicine & Pharmacotherapy, 57, 399–411.Google Scholar
  111. Teng, W., et al. (2013). Characterization of root response to phosphorus supply from morphology to gene analysis in field-grown wheat. Journal of Experimental Botany, 64, 1403–1411.Google Scholar
  112. Thompson, J., Clewett, T., & Fiske, M. (2013). Field inoculation with arbuscular-mycorrhizal fungi overcomes phosphorus and zinc deficiencies of linseed (Linum usitatissimum) in a vertisol subject to long-fallow disorder. Plant and Soil, 371, 117–137.Google Scholar
  113. Uauy, C., Distelfeld, A., Fahima, T., Blechl, A., & Dubcovsky, J. (2006). A NAC gene regulating senescence improves grain protein, zinc, and iron content in wheat. Science, 314, 1298–1301.Google Scholar
  114. Uygur, V., & Rimmer, D. (2000). Reactions of zinc with iron-oxide coated calcite surfaces at alkaline pH. European Journal of Soil Science, 51, 511–516.Google Scholar
  115. Vallee, B. L., & Auld, D. S. (1990). Zinc coordination, function, and structure of zinc enzymes and other proteins. Biochemistry, 29, 5647–5659.Google Scholar
  116. Vasconcelos, M., et al. (2003). Enhanced iron and zinc accumulation in transgenic rice with the ferritin gene. Plant Science, 164, 371–378.Google Scholar
  117. Verma, T., & Minhas, R. (1987). Zinc and phosphorus interaction in a wheat-maize cropping system. Nutrient Cycling in Agroecosystems, 13, 77–86.Google Scholar
  118. Verret, F., Gravot, A., Auroy, P., Leonhardt, N., David, P., Nussaume, L. (2004). Overexpression of AtHMA4 enhances root-to-shoot translocation of zinc and cadmium and plant metal tolerance. FEBS Letters, 576, 306–312.Google Scholar
  119. Warnock, R. (1970). Micronutrient uptake and mobility within corn plants (Zea mays L.) in relation to phosphorus-induced zinc deficiency. Soil Science Society of America Journal, 34, 765–769.Google Scholar
  120. Watts-Williams, S. J., Patti, A. F., & Cavagnaro, T. R. (2013). Arbuscular mycorrhizas are beneficial under both deficient and toxic soil zinc conditions. Plant and Soil, 371, 299–312.Google Scholar
  121. Watts-Williams, S. J., Smith, F. A., McLaughlin, M. J., Patti, A. F., & Cavagnaro, T. R. (2015). How important is the mycorrhizal pathway for plant Zn uptake? Plant and Soil, 390, 157–166.Google Scholar
  122. Watts-Williams, S. J., Turney, T. W., Patti, A. F., & Cavagnaro, T. R. (2014). Uptake of zinc and phosphorus by plants is affected by zinc fertiliser material and arbuscular mycorrhizas. Plant and Soil, 376, 165–175.Google Scholar
  123. Webb, M. J., & Loneragan, J. F. (1988). Effect of zinc deficiency on growth, phosphorus concentration, and phosphorus toxicity of wheat plants. Soil Science Society of America Journal, 52, 1676–1680.Google Scholar
  124. Webb, M. J., & Loneragan, J. F. (1990). Zinc translocation to wheat roots and its implications for a phosphorus/zinc interaction in wheat plants 1. Journal of Plant Nutrition, 13, 1499–1512.Google Scholar
  125. Welch, R. M., & Shuman, L. (1995). Micronutrient nutrition of plants. Critical Reviews in plant sciences, 14, 49–82.Google Scholar
  126. White, P. J., & Broadley, M. R. (2005). Biofortifying crops with essential mineral elements. Trends in Plant Science, 10, 586–593.Google Scholar
  127. White, P. J., & Broadley, M. R. (2009). Biofortification of crops with seven mineral elements often lacking in human diets—Iron, zinc, copper, calcium, magnesium, selenium and iodine. New Phytologist, 182, 49–84.Google Scholar
  128. White, P. J., & Broadley, M. R. (2011). Physiological limits to zinc biofortification of edible crops. Frontiers in plant science, 2, 1–11.Google Scholar
  129. Williams, L. E., & Mills, R. F. (2005). P 1B-ATPases–an ancient family of transition metal pumps with diverse functions in plants. Trends in Plant Science, 10, 491–502.Google Scholar
  130. Wissuwa, M., Ismail, A. M., & Yanagihara, S. (2006). Effects of zinc deficiency on rice growth and genetic factors contributing to tolerance. Plant Physiology, 142, 731–741.Google Scholar
  131. Yang, X., Li, T., Yang, J., He, Z., Lu, L., & Meng, F. (2006). Zinc compartmentation in root, transport into xylem, and absorption into leaf cells in the hyperaccumulating species of Sedum alfredii. Hance Planta, 224, 185–195.Google Scholar
  132. Yilmaz, A., Ekiz, H., Torun, B., Gultekin, I., Karanlik, S., Bagci, S., et al. (1997). Effect of different zinc application methods on grain yield and zinc concentration in wheat cultivars grown on zinc-deficient calcareous soils Journal of plant nutrition, 20, 461–471.Google Scholar
  133. Youngdahl, L., Svec, L., Liebhardt, W., & Teel, M. (1977). Changes in the zinc-65 distribution in corn root tissue with a phosphorus variable. Crop Science, 17, 66–69.Google Scholar
  134. Zhang, W., Liu, D., Liu, Y., Cui, Z., Chen, X., & Zou, C. (2016). Zinc uptake and accumulation in winter wheat relative to changes in root morphology and mycorrhizal colonization following varying phosphorus application on calcareous soil. Field Crops Research, 197, 74–82.Google Scholar
  135. Zhang, Y.-Q., et al. (2012). The reduction in zinc concentration of wheat grain upon increased phosphorus-fertilization and its mitigation by foliar zinc application. Plant and Soil, 361, 143–152.Google Scholar
  136. Zou, C., Qin, D., Xu, M., Shen, H., & Wang, B. (2001). Nitrogen, phosphorous and potassium uptake characteristics of rice and its relationship with grain yield. Journal of Nanjing Agricultural University, 25, 6–10.Google Scholar

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© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Nuclear Institute for Agriculture and Biology (NIAB)FaisalabadPakistan
  2. 2.Department of AgronomyUniversity of AgricultureFaisalabadPakistan

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